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Although originally thought to evolve clonally, studies have revealed that most bacteria exchange DNA. However, it remains unclear to what extent gene flow shapes the evolution of bacterial genomes and maintains the cohesion of species.

Here, we analyze the patterns of gene flow within and between >2600 bacterial species. Our results show that fewer than 10% of bacterial species are truly clonal, indicating that purely asexual species are rare in nature. We further demonstrate that the taxonomic criterion of ~95% genome sequence identity routinely used to define bacterial species does not accurately represent a level of divergence that imposes an effective barrier to gene flow across bacterial species. Interruption of gene flow can occur at various sequence identities across lineages, generally from 90 to 98% genome identity. This likely explains why a ~95% genome sequence identity threshold has empirically been judged as a good approximation to define bacterial species. Our results support a universal mechanism where the availability of identical genomic DNA segments required to initiate homologous recombination is the primary determinant of gene flow and species boundaries in bacteria. We show that these barriers of gene flow remain porous since many distinct species maintain some level of gene flow, similar to introgression in sexual organisms.

Overall, bacterial evolution and speciation are likely shaped by similar forces driving the evolution of sexual organisms. Our findings support a model where the interruption of gene flow—although not necessarily the initial cause of speciation—leads to the establishment of permanent and irreversible species borders.

Core genome phylogenies are widely used to build the evolutionary history of individual prokaryote species. By using hundreds or thousands of shared genes, these approaches are the gold standard to reconstruct the relationships of large sets of strains. However, there is growing evidence that bacterial strains exchange DNA through homologous recombination at rates that vary widely across prokaryote species, indicating that core genome phylogenies might not be able to reconstruct true phylogenies when recombination rate is high. Few attempts have been made to evaluate the robustness of core genome phylogenies to recombination, but some analyses suggest that reconstructed trees are not always accurate.

In this study, we tested the robustness of core genome phylogenies to various levels of recombination rates. By analyzing simulated and empirical data, we observed that core genome phylogenies are relatively robust to recombination rates; nevertheless, our results suggest that many reconstructed trees are not completely accurate even when bootstrap supports are high. We found that some core genome phylogenies are highly robust to recombination whereas others are strongly impacted by it, and we identified that the robustness of core genome phylogenies to recombination is highly linked to the levels of selective pressures acting on a species. Stronger selective pressures lead to less accurate tree reconstructions, presumably because selective pressures more strongly bias the routes of DNA transfers, thereby causing phylogenetic artifacts.

Overall, these results have important implications for the application of core genome phylogenies in prokaryotes.